Adding pieces to the puzzling plant nuclear envelope

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The nuclear envelope (NE) and the nuclear pores are important structures that both separate and selectively connect the nucleoplasm and the cytoplasm. NE and nuclear pore research in plants have recently seen an elevated level of interest. This is based both on new findings demonstrating the importance of nucleocytoplasmic trafficking for several signal transduction events, and on increasing evidence that NE and nuclear pore components play important roles during plant cell division. Here, we review the most recent reports in the field and compare them to the more advanced knowledge about yeast and animal model systems. They deal with the refined ultrastructure of the NE and NPC, with the discovery of novel NE components, and, importantly, with novel roles and fates of NE-associated and NPC-associated proteins during plant mitosis and cytokinesis.

Introduction

In eukaryotic cells, the nuclear envelope (NE) separates the nucleoplasm from the cytoplasm. The gateways for macromolecules through the NE are the nuclear pore complexes (NPCs), large multiprotein complexes of an eightfold symmetry embedded in the NE double membranes. Proteins and RNAs traffic through the NPCs, enabled by the interacting activities of the nuclear transport receptors (the karyopherins), the NPC proteins (Nups) and the elements of the Ran cycle (see Box 1, Figure I). In the animal and yeast fields, a combination of proteome, interactome, functional, and modeling studies are increasingly refining our understanding of the NPC (reviewed in [1]). Plant NE and NPC research is by comparison less advanced, in part based on the old expectation in the field that not much new could be learned by studying such a likely conserved cellular system. Over the past years, however, numerous reports have demonstrated that firstly, plants do not simply possess a carbon copy of the well-known animal and yeast systems [2, 3, 4, 5], and secondly, that both in plants [6] and in animals [7], NE and NPC biology hold more clues about regulation at the cellular and organismal level than previously anticipated. This renewed interest within the plant community is reflected in the number of exciting reports that have appeared in the past 18 months. They deal with the refined ultrastructure of the NE and NPC, with the discovery of novel NE components, and, importantly, with novel roles and fates of NE-associated and NPC-associated proteins during plant mitosis and cytokinesis (Table 1). Here, we focus on these new studies, while referring to recent reviews for plant work before the discussed time period [6, 8].

Section snippets

Ion channels

In animal cells, Ca2+ channels in the NE and ER are known to cause Ca2+ oscillations at the nuclear periphery. The channels are activated by secondary messengers such as IP3, which is liberated by phospholipase C [9]. In plants, Nod factor production by rhizobia causes two genetically separable Ca2+ responses, a rapid influx of calcium into root hair tips, and a slower appearance of calcium oscillations in the perinuclear region [10]. CASTOR and POLLUX were identified in mutant screens in Lotus

Conclusions

Much progress has been made in the past two to three years in determining components of the plant NPC and NE and in describing their contribution to diverse plant signaling processes (reviewed in [6]). In the meantime, however, the field has all but exploded in yeast and animal models, including precise structural models of the NPC, biophysical understanding of nucleocytoplasmic transport, the role of the NE in gene regulation and human disease, and the emerging evidence that nucleocytoplasmic

References and recommended reading

Papers of particular interest published within the period of review have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgement

Funding of our lab's research in this field by the National Science Foundation is greatly acknowledged.

References (57)

  • I. Meier

    Composition of the plant nuclear envelope: theme and variations

    J Exp Bot

    (2007)
  • T. Merkle

    Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling

    Curr Genet

    (2003)
  • Q. Zhao et al.

    Two distinct, interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP

    Plant Cell

    (2008)
  • M. Capelson et al.

    The role of nuclear pores in gene regulation, development and disease

    EMBO Rep

    (2009)
  • O. Gerasimenko et al.

    New aspects of nuclear calcium signalling

    J Cell Sci

    (2004)
  • H. Imaizumi-Anraku et al.

    Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots

    Nature

    (2005)
  • M. Charpentier et al.

    Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis

    Plant Cell

    (2008)
  • K. Krause et al.

    Nuclear regulators with a second home in organelles

    Trends Plant Sci

    (2009)
  • A. Fridkin et al.

    SUN-domain and KASH-domain proteins during development, meiosis and disease

    Cell Mol Life Sci

    (2009)
  • D. Van Damme et al.

    Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins

    Plant J

    (2004)
  • K. Roberts et al.

    Structure of the nuclear pore in higher plants

    Nature

    (1970)
  • J. Fiserova et al.

    Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells

    Plant J

    (2009)
  • K. Maeshima et al.

    Cell-cycle-dependent dynamics of nuclear pores: pore-free islands and lamins

    J Cell Sci

    (2006)
  • N. Belgareh et al.

    Dynamics of nuclear pore distribution in nucleoporin mutant yeast cells

    J Cell Biol

    (1997)
  • X.M. Xu et al.

    NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development

    Plant Cell

    (2007)
  • Y. Jacob et al.

    The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling

    Plant Physiol

    (2007)
  • A.K. McNulty et al.

    Purification and immunological detection of pea nuclear intermediate filaments: evidence for plant nuclear lamins

    J Cell Sci

    (1992)
  • A. Minguez et al.

    Immunological characterization of lamins in the nuclear matrix of onion cells

    J Cell Sci

    (1993)
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